Functional excitatory GABAA receptors precede ionotropic glutamate receptors in radial glia-like neural stem cells

Molecular and Cellular Neuroscience

Volumn 43, Issue 2, 2010, Pages 209-221

  Muth Köhne, Elke ^a   Terhag, Jan ^a   Pahl, Steffen ^a   Werner, Markus ^a   Joshi, Illah ^a   Hollmann, Michael ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

AMPA receptors; GABAA receptors; In vitro differentiation; Neural stem cells; NMDA receptors

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA 2 PROTEIN; 4 AMINOBUTYRIC ACID A RECEPTOR BETA 3 PROTEIN; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA 1 PROTEIN; 4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; IONOTROPIC RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3A; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; BICUCULLINE; ENHANCED GREEN FLUORESCENT PROTEIN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; N METHYLASPARTIC ACID; NR1 NMDA RECEPTOR; NR2B NMDA RECEPTOR; POTASSIUM CHANNEL BLOCKING AGENT; PROTEIN SUBUNIT; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1 PROTEIN; SODIUM-POTASSIUM-CHLORIDE COTRANSPORTER 1 PROTEIN; SOX1 PROTEIN, MOUSE; TETRYLAMMONIUM; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL POPULATION; CONTROLLED STUDY; EMBRYO; GENE OVEREXPRESSION; GLIA CELL; IMMUNOBLOTTING; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NEURAL STEM CELL; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTOGENESIS; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CELL DIFFERENTIATION; CELL MEMBRANE POTENTIAL; DRUG EFFECT; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GLIA; METABOLISM; METHODOLOGY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; BICUCULLINE; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; N-METHYLASPARTATE; NEUROGENESIS; NEUROGLIA; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; PROTEIN SUBUNITS; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SOXB1 TRANSCRIPTION FACTORS; TETRAETHYLAMMONIUM; TRANSFECTION;

EID: 73049110753     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.11.002     Document Type: Article

References (90)

1. Aubert J., Stavridis M.P., Tweedie S., O'Reilly M., Vierlinger K., Li M., Ghazal P., Pratt T., Mason J.O., Roy D., and Smith A. Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc. Natl. Acad. Sci. U. S. A. 100 Suppl 1 (2003) 11836-11841
2. Barria A., and Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48 (2005) 289-301
3. Behe P., Stern P., Wyllie D.J., Nassar M., Schoepfer R., and Colquhoun D. Determination of NMDA NR1 subunit copy number in recombinant NMDA receptors. Proc. Biol. Sci. 262 (1995) 205-213
4. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev., Neurosci. 3 (2002) 728-739
5. Ben-Ari Y., Khazipov R., Leinekugel X., Caillard O., and Gaiarsa J.L. GABAA, NMDA and AMPA receptors: a developmentally regulated 'menage a trois'. Trends Neurosci. 20 (1997) 523-529
6. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
7. Blitzer R.D., Connor J.H., Brown G.P., Wong T., Shenolikar S., Iyengar R., and Landau E.M. Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280 (1998) 1940-1942
8. Bolteus A.J., and Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 24 (2004) 7623-7631
9. v channels in cultured astrocytes. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 9336-9340
10. Borodinsky L.N., Root C.M., Cronin J.A., Sann S.B., Gu X., and Spitzer N.C. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429 (2004) 523-530
11. Bovolin P., Santi M.R., Puia G., Costa E., and Grayson D. Expression patterns of gamma-aminobutyric acid type A receptor subunit mRNAs in primary cultures of granule neurons and astrocytes from neonatal rat cerebella. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 9344-9348
12. Brown G.P., Blitzer R.D., Connor J.H., Wong T., Shenolikar S., Iyengar R., and Landau E.M. Long-term potentiation induced by theta frequency stimulation is regulated by a protein phosphatase-1-operated gate. J. Neurosci. 20 (2000) 7880-7887
13. Cameron H.A., McEwen B.S., and Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15 (1995) 4687-4692
14. Cameron H.A., Hazel T.G., and McKay R.D. Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36 (1998) 287-306
15. Cancedda L., Fiumelli H., Chen K., and Poo M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27 (2007) 5224-5235
16. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., and Nicoll R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 (2000) 936-943
17. Chen Y., Beffert U., Ertunc M., Tang T.S., Kavalali E.T., Bezprozvanny I., and Herz J. Reelin modulates NMDA receptor activity in cortical neurons. J. Neurosci. 25 (2005) 8209-8216
18. Ciabarra A.M., Sullivan J.M., Gahn L.G., Pecht G., Heinemann S., and Sevarino K.A. Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J. Neurosci. 15 (1995) 6498-6508
19. Conti L., Pollard S.M., Gorba T., Reitano E., Toselli M., Biella G., Sun Y., Sanzone S., Ying Q.L., Cattaneo E., and Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 3 (2005) e283
20. Deisseroth K., Singla S., Toda H., Monje M., Palmer T.D., and Malenka R.C. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42 (2004) 535-552
21. 2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36 (2002) 1051-1061
22. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51 (1999) 7-61
23. Esposito M.S., Piatti V.C., Laplagne D.A., Morgenstern N.A., Ferrari C.C., Pitossi F.J., and Schinder A.F. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25 (2005) 10074-10086
24. Esteban J.A., Shi S.H., Wilson C., Nuriya M., Huganir R.L., and Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 6 (2003) 136-143
25. Farrant M., Feldmeyer D., Takahashi T., and Cull-Candy S.G. NMDA-receptor channel diversity in the developing cerebellum. Nature 368 (1994) 335-339
26. Fiszman M.L., Borodinsky L.N., and Neale J.H. GABA induces proliferation of immature cerebellar granule cells grown in vitro. Brain Res. Dev. Brain Res. 115 (1999) 1-8
27. Ganguly K., Schinder A.F., Wong S.T., and Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105 (2001) 521-532
28. Ge S., Goh E.L., Sailor K.A., Kitabatake Y., Ming G.L., and Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439 (2006) 589-593
29. Glaser T., Pollard S.M., Smith A., and Brustle O. Tripotential differentiation of adherently expandable neural stem (NS) cells. PLoS ONE 2 (2007) e298
30. Goffin D., Aarum J., Schroeder J.E., Jovanovic J.N., Richardson J.C., and Chuang T.T. D1-like dopamine receptors regulate GABAA receptor function to modulate neuroprogenitor cell proliferation. Neuroscience Meeting Planner 2007 (2007), Society for Neuroscience, San Diego, CA
31. Gotz M., and Huttner W.B. The cell biology of neurogenesis. Nat. Rev., Mol. Cell Biol. 6 (2005) 777-788
32. Gubellini P., Ben-Ari Y., and Gaiarsa J.L. Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus. Eur. J. Neurosci. 14 (2001) 1937-1946
33. Hall B.J., and Ghosh A. Regulation of AMPA receptor recruitment at developing synapses. Trends Neurosci. 31 (2008) 82-89
34. Hevers W., and Luddens H. The diversity of GABAA receptors. Pharmacological and electrophysiological properties of GABAA channel subtypes. Mol. Neurobiol. 18 (1998) 35-86
35. Hirasawa T., Wada H., Kohsaka S., and Uchino S. Inhibition of NMDA receptors induces delayed neuronal maturation and sustained proliferation of progenitor cells during neocortical development. J. Neurosci. Res. 74 (2003) 676-687
36. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994) 31-108
37. Iwamoto T., Yamada Y., Hori K., Watanabe Y., Sobue K., and Inui M. Differential modulation of NR1-NR2A and NR1-NR2B subtypes of NMDA receptor by PDZ domain-containing proteins. J. Neurochem. 89 (2004) 100-108
38. Jelitai M., Schlett K., Varju P., Eisel U., and Madarasz E. Regulated appearance of NMDA receptor subunits and channel functions during in vitro neuronal differentiation. J. Neurobiol. 51 (2002) 54-65
39. Kitayama T., Yoneyama M., and Yoneda Y. Possible regulation by N-methyl-d-aspartate receptors of proliferative progenitor cells expressed in adult mouse hippocampal dentate gyrus. J. Neurochem. 84 (2003) 767-780
40. Kitayama T., Yoneyama M., Tamaki K., and Yoneda Y. Regulation of neuronal differentiation by N-methyl-d-aspartate receptors expressed in neural progenitor cells isolated from adult mouse hippocampus. J. Neurosci. Res. 76 (2004) 599-612
41. Laemmli U.K., Cheng S.M., Adolph K.W., Paulson J.R., Brown J.A., and Baumbach W.R. Metaphase chromosome structure: the role of nonhistone proteins. Cold Spring Harbor Symp. Quant. Biol. 42 Pt 1 (1978) 351-360
42. Laube B., Kuhse J., and Betz H. Evidence for a tetrameric structure of recombinant NMDA receptors. J. Neurosci. 18 (1998) 2954-2961
43. Levitt P., Harvey J.A., Friedman E., Simansky K., and Murphy E.H. New evidence for neurotransmitter influences on brain development. Trends Neurosci. 20 (1997) 269-274
44. Li P., and Zhuo M. Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature 393 (1998) 695-698
45. Liebau S., Propper C., Bockers T., Lehmann-Horn F., Storch A., Grissmer S., and Wittekindt O.H. Selective blockage of Kv1.3 and Kv3.1 channels increases neural progenitor cell proliferation. J. Neurochem. 99 (2006) 426-437
46. Liu X., Wang Q., Haydar T.F., and Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 8 (2005) 1179-1187
47. LoTurco J.J., Owens D.F., Heath M.J., Davis M.B., and Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15 (1995) 1287-1298
48. Luk K.C., and Sadikot A.F. Glutamate and regulation of proliferation in the developing mammalian telencephalon. Dev. Neurosci. 26 (2004) 218-228
49. Luk K.C., Kennedy T.E., and Sadikot A.F. Glutamate promotes proliferation of striatal neuronal progenitors by an NMDA receptor-mediated mechanism. J. Neurosci. 23 (2003) 2239-2250
50. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., and Gotz M. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37 (2003) 751-764
51. Malenka R.C., and Nicoll R.A. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 16 (1993) 521-527
52. Manent J.B., Demarque M., Jorquera I., Pellegrino C., Ben-Ari Y., Aniksztejn L., and Represa A. A noncanonical release of GABA and glutamate modulates neuronal migration. J. Neurosci. 25 (2005) 4755-4765
53. Mano I., and Teichberg V.I. A tetrameric subunit stoichiometry for a glutamate receptor-channel complex. NeuroReport 9 (1998) 327-331
54. Merkle F.T., Tramontin A.D., Garcia-Verdugo J.M., and Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 17528-17532
55. Mizielinska S., Greenwood S., and Connolly C.N. The role of GABAA receptor biogenesis, structure and function in epilepsy. Biochem. Soc. Trans. 34 (2006) 863-867
56. + channel and GABAA receptor expression in Bergmann glial cells. J. Neurosci. 14 (1994) 2503-2514
57. Nacher J., Rosell D.R., Alonso-Llosa G., and McEwen B.S. NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur. J. Neurosci. 13 (2001) 512-520
58. Nguyen L., Rigo J.M., Rocher V., Belachew S., Malgrange B., Rogister B., Leprince P., and Moonen G. Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305 (2001) 187-202
59. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., and Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22 (2002) 3161-3173
60. Owens D.F., and Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat. Rev., Neurosci. 3 (2002) 715-727
61. Pardo L.A. Voltage-gated potassium channels in cell proliferation. Physiology (Bethesda) 19 (2004) 285-292
62. Park M., Penick E.C., Edwards J.G., Kauer J.A., and Ehlers M.D. Recycling endosomes supply AMPA receptors for LTP. Science 305 (2004) 1972-1975
63. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
64. Pollard S.M., Conti L., Sun Y., Goffredo D., and Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb. Cortex 16 Suppl. 1 (2006) i112-120
65. Poulsen F.R., Blaabjerg M., Montero M., and Zimmer J. Glutamate receptor antagonists and growth factors modulate dentate granule cell neurogenesis in organotypic, rat hippocampal slice cultures. Brain Res. 1051 (2005) 35-49
66. Rajan I., and Cline H.T. Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J. Neurosci. 18 (1998) 7836-7846
67. Rakic P. Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 11323-11327
68. Ripellino J.A., Neve R.L., and Howe J.R. Expression and heteromeric interactions of non-N-methyl-d-aspartate glutamate receptor subunits in the developing and adult cerebellum. Neuroscience 82 (1998) 485-497
69. Riquelme R., Miralles C.P., and De Blas A.L. Bergmann glia GABA(A) receptors concentrate on the glial processes that wrap inhibitory synapses. J. Neurosci. 22 (2002) 10720-10730
70. - cotransporter KCC2 and carbonic anhydrase CAVII. J. Physiol. 562 (2005) 27-36
71. - cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons. J. Neurosci. 16 (1996) 82-91
72. Rosenmund C., Stern-Bach Y., and Stevens C.F. The tetrameric structure of a glutamate receptor channel. Science 280 (1998) 1596-1599
73. Rougon G., Dubois C., Buckley N., Magnani J.L., and Zollinger W. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol. 103 (1986) 2429-2437
74. Sadikot A.F., Burhan A.M., Belanger M.C., and Sasseville R. NMDA receptor antagonists influence early development of GABAergic interneurons in the mammalian striatum. Brain Res. Dev. Brain Res. 105 (1998) 35-42
75. Sans N., Petralia R.S., Wang Y.X., Blahos II J., Hell J.W., and Wenthold R.J. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20 (2000) 1260-1271
76. Sans N., Prybylowski K., Petralia R.S., Chang K., Wang Y.X., Racca C., Vicini S., and Wenthold R.J. NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell Biol. 5 (2003) 520-530
77. Schlett K. Glutamate as a modulator of embryonic and adult neurogenesis. Curr. Top. Med. Chem. 6 (2006) 949-960
78. Schmidt-Hieber C., Jonas P., and Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429 (2004) 184-187
79. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., and Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284 (1999) 1811-1816
80. Spitzer N.C., and Lamborghini J.E. The development of the action potential mechanism of amphibian neurons isolated in culture. Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 1641-1645
81. Stavridis M.P., and Smith A.G. Neural differentiation of mouse embryonic stem cells. Biochem. Soc. Trans. 31 (2003) 45-49
82. Sucher N.J., Akbarian S., Chi C.L., Leclerc C.L., Awobuluyi M., Deitcher D.L., Wu M.K., Yuan J.P., Jones E.G., and Lipton S.A. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J. Neurosci. 15 (1995) 6509-6520
83. Takahashi Y., Tsumoto T., and Kubo T. N-methyl-d-aspartate receptors contribute to afferent synaptic transmission in the medial vestibular nucleus of young rats. Brain Res. 659 (1994) 287-291
84. Tomita S., Chen L., Kawasaki Y., Petralia R.S., Wenthold R.J., Nicoll R.A., and Bredt D.S. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol. 161 (2003) 805-816
85. Tovar K.R., and Westbrook G.L. Mobile NMDA receptors at hippocampal synapses. Neuron 34 (2002) 255-264
86. Tozuka Y., Fukuda S., Namba T., Seki T., and Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47 (2005) 803-815
87. Wang L.P., Kempermann G., and Kettenmann H. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol. Cell. Neurosci. 29 (2005) 181-189
88. Weissman T.A., Riquelme P.A., Ivic L., Flint A.C., and Kriegstein A.R. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43 (2004) 647-661
89. Wong H.K., Liu X.B., Matos M.F., Chan S.F., Perez-Otano I., Boysen M., Cui J., Nakanishi N., Trimmer J.S., Jones E.G., Lipton S.A., and Sucher N.J. Temporal and regional expression of NMDA receptor subunit NR3A in the mammalian brain. J. Comp. Neurol. 450 (2002) 303-317
90. Ying Q.L., Stavridis M., Griffiths D., Li M., and Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21 (2003) 183-186